MARINE ECOLOGY PROGRESS SERIES Mar Ecol Prog Ser Vol. 160: 109-120.1997 Published December IS Natural variation of radionuclide 1 3 7 concentration ~s in marine organisms with special reference to the effect of food habits and trophic level Fujio Kasamatsu*,Yusuke Ishikawa Marine Ecology Research Institute, Tokyo Head Office, Teikoku Shoin Bldg, 3-29 Jinbo-cho, Kanda, Chiyoda, Tokyo 101, Japan ABSTRACT. Although a number of measurements have been made on radiocesium concentrations in aquatic organisms, no clear agreement has been reached on the factors affecting accumulation of these radionuclides. Natural variations in the concentration of the long-lived artificial radionuclide '37Cs in marine organisms and factors affecting variations in marine fishes were investigated through long-term and systematic measurements in coastal waters of Japan from 1984 to 1995. Concentrations of 13'Cs were measured in more than 30 species of crustaceans, cephalopods and teleosts considered representative of the marine biotic community. A clear positive correlation (p < 0.05) was found between mean weight and concentration of 137Csin 276 fish samples. However, different relationships between 137Cs concentration and weight of fish were observed in different species. Within 16 studied species I3'cs concentration increased with growth for 4 species, while no specific correlation was observed in the remaining species. These different patterns depended on a change of food habits with growth. Analysis of 6066 stomach contents of fish samples together with '37Csconcentrations in the stomach contents demonstrated that 137Csconcentration increased with rising trophic level and that the biomagnification factor (13'cs in p r e d a t ~ r / ' ~ ~in C sprey) was 2.0 (95% confidence interval 1.8 to 2.2). From the yearly change of '37Cs in 24 marine fish species, a mean effectlve environmental half-life of I3'Cs of 13 * 3 yr (range 10 to 17 yr) was calculated. KEY WORDS: Trophic level . Food habits . Marine dependence . Environmental half-life INTRODUCTION The long-lived artificial radionuclide 137Cscan be considered to be of great interest and importance as an indicator of radioactive pollution in the marine environment because of its relatively high radiotoxicity. Its major sources are the atmospheric deposition of debris from past nuclear explosions during 1954 to 1962 and 1980. The nuclear accident at the Chernobyl nuclear power station has renewed interest in this radionuclide. The fate and cycling of radionuclides in ecosystems have long been a subject of major interest to applied ecologists and health physicists. Although many mea- O Inter-Research 1997 Resale of full article not permitted organisms . Bioaccumulation . I3'Cs , Size- surements have been made on radiocesium concentrations and their variations in aquatic organisms (e.g. Williams & Pickering 1961, Baptist & Price 1962, Hiyama & Shimizu 1964, King 1964, Morgan 1964, Hasanen et al. 1968, Kolehmainen et al. 1968, Jefferies & Hewett 1971, Pentreath & Jefferies 1971, Whicker et al. 1972, Pentreath 1973, Suzuki et al. 1973, Newman & Brisbin 1990, Tateda & Misonou 1991, Morgan et al. 1993, Cocchio et al. 1995),no agreement seems to have been reached on the factors affecting the accumulation of this radionuclide, and this lack of ecological understanding has hindered the development of a robust dose model (Rowan & Rasmussen 1994). Furthermore, the bioaccun~ulationof radionuclides by aquatic organisms and the factors affecting the concentrations have been examined mainly under controlled conditions in aquaria. Such studies have been 110 Mar Ecol Prog Ser 160: 109-120, 1997 conducted on a limited range of marine species (generally species easy to rear in laboratory expenments) and performed under conditions that cannot be truly representative of the natural environment. There have been few direct and large-scale environmental studies on '37Csaccumulation in marine organisms in the natural environment. Although there is a general agreement that food is the major route of I3'Cs uptake by fish, some authors claim varying degrees of biomagnification (Gustafson 1967), some deny food-chain effects (Reichle et al. 1970, Thomann 1981), and some even claim that the radiocesium undergoes 'biodiminution' in aquatic food chains (Mailhot et al. 1988). The Marine Ecology Research Institute, Tokyo, has been carrying out large-scale and systematic measurements of '37Cs concentrations of sea water, sediments and marine edible organisms sampled from fishing grounds along the coast of Japan since 1984 as part of a n extended marine environmental radioactive monitoring program sponsored by the Science and Technology Agency of Japan. This paper reports the variation of '37Csin edible marine organisms, with special reference to the factors affecting 13?Csconcentration, based on results from the long-term measurements at different locations around Japan over more than 10 yr (1984 to 1995). 24 h. Samples were analyzed using Gamma-spectrometry to determine 137Cs(measuring for 20 h ) . Results were expressed as Bq kg-' wet weight for I3?Cs. 13?cs concentrations in sea water were measured from 50 1 samples. Cesium was absorbed onto ammonium molybdophosphate precipitate under acidic conditions, and 137Cswas separated by means of a cation exchange resin column method, fixed as cesium chloroplatinate and measured by Gamma-spectrometry (measuring for 20 h). Food habits of the studied fish species were investigated from their stomach contents. Stomach contents were expressed as a percentage of weight of each prey item against total weight of stomach contents. RESULTS Variation oi 13'Cs concen1ra:ions in marine organisms Table 1 shows details of the marine organisms analyzed from 1984 to 1995, together with their concentrations of 137Csand mean concentration factors (CF; concentration in organism/concentration in sea water) of 13'Cs during the years 1992 to 1995. Tables 2 & 3 shows MATERIALS AND METHODS Sampling areas and samples. The locations of sampling sites are shown in Fig. 1. For the purpose of the monitoring program, marine organisms to be analyzed were selected from coastal species which have been abundantly caught by the coastal fisheries of Japan. Marine organism samples were taken on the continental shelf and shelf slope (between the sea surface and approximately 500 m depth) around Japan, through various fishing operations. These samples were provided twice a year by the local fisherman's union. Samples of marine organisms were frozen and transferred to the laboratory. More than 30 species (representing more than 20 families) of marine organisms were sampled. The samples consisted of teleosts, cephalopods and crustaceans. The species and samples measured during 1984 to 1995 are shown in Table 1. Sea water was sampled once a year using a Niskin type bottle, taking 80 1 per sample. Measurement. Samples of marine organisms (total wet weight about 20 kg) were transported to the Japan Chemical Analysis Center, where the major part of the analysis was carried out. Muscle tissues from each fish were dissected out and pooled. After being dried at 105"C, individual samples were ashed at 450°C for P4ClFlC OCEAN 'W Kagoshi ma 0Sampling area for organisms samples Sarnpl~ngsrarion for sea warer samples Nuclear power plant Fig. 1. Sampling sites in Japan Kasamatsu & Ishikawa: '37Csconcentrations In m a n n e organisms 111 :able 1. Length, wet welght and concentration of '"CS in marine organisms measured during 1984 to 1995. CF: concentration facor (concentration in organism/concentration in sea water). ND: not detected; concentration less than 3 times the analysis errors Species Chondrichthyes Order Rajiformes Family Dasyatididae Stingrays Osteichthyes Order Anguiliformes Family Congridae Common Japanese conger Order Salmon~formes Family Argentlnldae Deep-sea smelt Order Gadlformes Family Mondae Mond cod Family Gadidae Pacific cod Walleye pollack Order Scorpaeniformes Family Scorpaenidae Scorpion fish Black rockfish Family Platycephalidae Bertail flathead Family Hexagrammldae Atka mackerel Greenling Order Perciformes Family Perc~chthyidae Japanese sea bass Family Carangidae Jacks Family Spandae Red sea bream Crimson sea bream Yellow sea bream Family Sciaenidae White croaker Black mouth croak Family Girellidae Rudder fish Family Trichodontidae Japanese sandfish Order Pleuronectiforms Family Paralichthyidae Bastard halibut Family Pleuronectidae Flathead flounder Pointhead flounder Shothole halibut Stone flounder Brown sole Marbled sole Rikuzen sole Family Cynogloss~dae Black tonguefish Red tonguef~sh Cephalopods Family Decapoda Family Octopoda Crustacea Family Decapoda No. of samples Mean length Max. Min. (cm) Mean wet weight Max. Min. (g) Concentration Max. Min. (Bq kg-' fresh) Mean C F & SD 1992-95 112 Mar Ecol Prog Ser 160: 109-120, 1997 -- mean concentrations of '"CS in sea water (0 to 200 m depth) during the period 1984 to 1995 (14 sites with 56 stations) and '"'CS in sea water by depth (1992 to 1995), respectively. Concentration of I3'Cs in fishes ranged from 0.05 to 0.74 Bq kg-' fresh wt ( n = 746) during 1984 to 1995 and the 1992-95 overall mean concentration factor was 59 + 24 (n = 276). Concentration of 137Csin squids varied from ND (not detected) to 0.09 Bq kg-' fresh wt (n = 53), and that of octopus from ND to 0.09 Bq kg-' fresh wt (n = 89). Concentration of '37Csin shrimps (Crustacea Decapoda) ranged from 0.04 to 0.19 Bq kg-' fresh wt (n = 23) with 1992-1995 mean CF of 26 + 10 ( n = 31). Table 2. Mean concentrations of ' " ~ C S in the coastal surface sea water ( 0 to 200 m depth) Year '"CS SD (mBq I-') No. of samples Sampl~ng penod Mar-Dec Jun-Aug May-Jul May-Rug May-Jul May-Jul May-Jul May-Jul May-Jul May-Jun May-Jul May-Jul Effect of a r e a on '37Cs concentration The possible effect of area of origin on the concentrations of '"CS was investigated by comparing concentrations by areas and by species (Table 4 ) . Table 3 . Mean concentrations of '"'CS of sea water by depth in There were no significant differences in the concencoastal waters during 1992 to 1995 trations between areas except in 2 species, Atka mackerel Pleurogrammus azonus and common Japanese Depth :17cS SD No. of conger Conger myriaster. There was no difference in (m) (mBq I-') samples the depth of habitats and the I3'Cs concentrations of 0-200 3.15 0.35 416 the sea waters between the areas (Kasamatsu & Inatom 34 200-300 2.75 0.57 1997). In the case of the common Japanese conger, 300-400 2.42 0.40 24 however, a large difference in size between areas was 400-520 1.90 0.33 23 noted. The concentration of "'CS in this species is sizedependent (as discussed in the following section). A possible reason for the difference in '37Cs concentration in Table 4. Mean concentration factors of '"CS in 7 species from different areas. CF: concentration factor Atka mackerel between areas is also explained in the 'Discussion'. Effect of fish size on 13'Cs concentration Fig. 2 shows the relationship between mean CF of '37Csand the mean total length and the mean body weight for 28 fish species (147 samples) obtained during 1992 to 1.995. There was a clear positive correl.ation (the slopes are significantly different from zero at 5 % level). This demonstrates that the heavier and bigger species in the marine fish community apparently have the higher concentration factor of '37Cs. Fig. 3 shows the relationship between mean CF of I3'Cs and mean body weight for the 14 major fish species studied. Within these 14 spe- Species Sampling area I3'Cs CF 2 SD Walleye pollack Hokkaido Niigata 96 + 11 95 + 7 Japanese sea bass Fukushima Fukui Saga Bastard halibut Hokkaido lbaraki Fukui Shlmane Atka mackerel Hokkaido Niigata Japanese common conger Miyagi Fu kui Red sea bream Shlmane Fukui Pacific cod Miyagi Fukushima 'Signif~cantlydifferent at 5'%,level, "at 1 No. of samples level Mean weight + S D (g) suo!lelluasuo3 q61q '1elauab u~ ' ~ 3 30 s u o ~ ~ e . ~ ~ ueaw u a ~ uqol~! ~iaqla6ol 0z iorew aql JO uo!1!soduro3 lual s a p a d s O J O J j q 6 ! a ~ hp0q UeaU -uos y3eurols aql s ~ o q ps '61g '(S a ~ q e ~ ) PUP SaLCI 10 SlOl3PJ U011 -eJluaxoJ ueaur uaaM1 palnspaur osle aiaM qseutols aql WOJJ -aq sd!qsuorle[a~.E . 6 ! ~ A1~3a~!ppalsaIIos sdnoi6 L a ~ dasaql U! s3L61JO S U O J ~ ~ I I U ~ .(e~aey3d1od ~ U O ~ 09 l L[u!ewr) soqiuaq-oiseu~pue u o ~ y u e ~ d ( 3 ) lqZ!aM L P ~ € I -002 'spodo~eqdas'suea3elsnn p o d w 001 000s OOSZ 0 3 YSIJ IPIS '(q16ua1 1~101 -ap ' ( ~ SI>) u s SI<) q s ! ~a61el :sa!lo6ale~~ U ~ M O [ ~ O J aql o~u! pagyssep aJaM slualuo3 q3e -urols aql UI swal! Aaid aqL .sBuuds z pue suwnlne :suoseas g paluasaidal s a ~ d w e sa q l .sapads sz wolj s.[enp!lz -1pu1 9909 UI p a u ~ w a x aaJaM slualuo3 rl3e~uols ' ~ 6 6 501 c661 6urinp pale6 0 0081 006 0 -!lsaAu! sew says!$ u1 uo1~ei~ua3uo3 0 s3Lc,ay] uo suqeq POOJ JO 13aJJaarlL ( 8 1 I Y ~ ! ~6poa M ( 8 1 l q s ! a ~Lpoa OS2 001 000c OOSI 00s OOE 001 008 OSP 009 OOt OOP 0 00P elep ay1 01 slrj saienbs ]sea1 aJe s a u g .sapads qs!~ p1 0 002 El ureaJq eas uosmu3 OOSS 00s 0091 008 0 waJq cas pax 09 1 00s sseq eas asauedel m 008 000 0 qsy U O ! & O ~ ~ - 0009 OOSE 0001 006 0 - 09 1 OS0 0 .sapads bug~!eura~ aql U! pag!$uapy seM uo!lqalJos s!jpads ON .,ru,rajsuazray epueur17 a1os u ~ o l qpue 'snlqnp sapro -sso[.6oddr~lapunoj peaqJeU 'ejejsund P[[arrg ysrj lappnr 'slurlaut sajseqas qs!jy301 y s e ~ qaql 10j paAiasqo SPM l y 6 1 a ~J O aseanu! q l ~ uo!lellua3uos ~ t ON .sniero[osrqs n r a r q s3,,, J O asea.13~1 iapunolj auojs pup sn3cpu.r snleydas - 4 s peaqlelj ~ Irpliaq 'snleydasorseul snpe3 p03 s1~1sed' ~ a 6 u o 3asaueder uourwros ay] 103 pailiasqo SPM (10.0 > d) uo!lalallos a~!j!sod ~ U P X J ! U ~ I S e ' s a p elep aq] 01 slg s a ~ e n b ps e a l aIe s a u q ' ~ 6 6 1 - ~ 6 66uunp 1 s a ~ d w e sqsrj t p jo~ i q 6 ! a ~dpoq pue ql6ua1 [PIOI ueaw pue s3,= JO sJopej u o ~ l e i l u a ~ uueaur o ~ uaamlaq sd~qsuo!lelaa .Z ,613 ~ ~ ~ Mar Ecol Prog Ser 160: 109-120, 1997 s In stomach contents. CF: concentration factor Table 5. i ' i 7 ~concentrations Stomach contents Flsh (large size) F ~ s h(small SIX) Fish (combined) Crustacean Decapoda Cephalopoda Benthos Zooplankton 1 ' ' 7 ~ s 4(CF) ( B q kg-'] * 0.15 0.01 (481 0.10 ? 0.01 (321 0.12 0.01 (38) 0.1 1 0.01 (35) 0.03 0.01 (10) * * * Major contents Horse mackerel etc. Sandlance, anchovy etc, Prawn, shrimp Squid Polychaetes Euphausiacea I3'Cs CF from literatureh 56 * 24 (this work) 30 t 6 (11, (this work) 34 * 13 (i],(this work) 26 * 10 ( t h ~work) s 17 ? 13 (iii] 4 8 *2 (11) * 5-15 (I, iii) dValues are shown i analysis error "Literature. (i) Ibaralu Environmental Pollution Research Center (1993, 1994, 1995);(ii)Pentreath & Jeffenes (1971);(iii) Gomez et al. (1991) Fig. 4. Stomach contents and '37Cs concentrations of 20 fish species. (H) Hokkaido; (N) Niigata; (L) large; (S) small Kasamatsu & Ishikawa: I3'Cs concentrations In marine organisms 115 were observed in fish species whose prey was large-size fishes (e.g. Japanese sea bass and Pacific cod) and low concentrations were observed in fish species whose prey was mainly macro-benthos (e.g.brown sole and red tonguefish). It was, however, noted that relatively high concentrations were observed in Atka mackerel, walleye pollack and deep-sea smelt Glossanodon semifasciata and that the food of these fishes was not from the high trophic levels. Fig. 5 shows stomach contents in relation to body size (at different growth stages) for 9 major fish species. With increase of body size (with growth) Pacific cod, stone flounder, Japanese common conger and bertail flathead apparently change their prey from that of low trophic level to that of high trophic level. I3'Cs in these species tends to increase with increase in size. In contrast, within the examined range of weight, flathead flounder, brown sole, Japanese sea bass and red sea bream do not change their food habits. These observations suggested that the size-dependent concentration of '37Cs is mainly due to change of food habit. A quantitative examination of the relationship between the concentration of 1 3 7 ~ins food and in fish was carried out. '37Cs in the intake-food (I)is here expressed as follows: where bi is the absorption percentage of 137Cs for the ith food item,. di. is the concentration of Crustacca l&Ccphal@ 13'Cs in the ith food item (Table 5), and f , is the Fish(L) MacroFish(S) bcnthos proportion of the ith food item in the diet of fish Fig. 5. Stomach contents of different body size ranges for the major (Reichle 1969, Kolehmainen 1974). An absorp9 species tion of 90% was assumed. Fig. 6 shows the relationship between '37Cs in the intake-food and '37Cs in the fishes that inhabit surface layers (above 0.4 W fishes in surface lasers approximately 150 m depth, closed circles in Fig. 6). A 0 fishes in dccprvalcr significant positive relationship (r = 0.79, p < 0.001) o --, 0.3 was observed, suggesting food habits to be the major 0 factor affecting concentration of 137Csin fishes, and the biomagnification factor (13'Cs in predator/13'Cs in c 2 0.2 prey) was estimated at 2.0 (95% confidence interval .-C 1.8 to 2.2). m$;,On g,ccapoda - /' d z- 0.1 - m m Effect of habitat on concentration Fig. 7 shows depths of habitats and '"CS concentrations of 21 fish species samples. From the observations presented in Figs. 6 & 7, it is noted that walleye pollack, ~ t k mackerel a and deep-sea smell that inhabit a depth of 150 to 400 m with lower sea temperature have high concentrations of '"CS despite low concentra- y=ZOz: O . 0.00 O j - . 0.05 CS in food (Bq/kg) 137 , R' =0.63 , I 0.10 ~i~ 6, ~ ~ l ~of 13'~s l ~concentration ~ ~ ~ between h i foodr ~ and fishes. ( 0 ) Fishes in surface layers, (0)fishes in deep-sea waters (walleye pollack, Atka mackerel and deep-sea smelt) Mar Ecol Prog Ser 160: 109-120, 1997 116 30 38 57 54 9: Concentrat~onFactor 16 27 l ? 37 59 66 51 50 70 7 s 50 8C !? 73 76 94 weight were excluded to avoid sizedependent effects. The effective environmental half-lives range from 10 to 17 yr w ~ t ha mean of 13 + 3 yr (Table 6). These half-l~ves were slightly lower than those determined in surface layers of sea water (16 to 18 yr; Kasamatsu & Inatomi 1997) but not significantly different. DISCUSSION Flg 7 Depth of capture a n d I3'Cs concentration factors of the 21 fish species studled Closed clrcles show depth of capture a n d vertlcal llnes show range of depth from the literature Depths of captures were provlded from lntervlews with fishermen conducted during 1994 Radiocesium '"CS falls to earth in a readily soluble form following atomic bomb detonations and is thus available to human beings through concentration and transfer up the food chain. Identification of factors affecting or controlling accumulations of 13?Cs in edible marlne organisms is critically necessary to identify pathways of radiocesium accumulation from a surface input. Factors affecting accumulation of I3jCs in fishes have been the subject of previous investigations (Bryan 1963, tions in their food and in environmental sea water (see Table 3). Concentration factors along trophic level L Our investigations indicated that food habit was one of the most important factors affecting concentrations of 13'cs in m a n n e flshes, a n d Fig 8 shows the relationship between the 13jCs concentration factor and the oceanic food chains A clear Increase in the concentration factor was observed with Increase In trophic level Nevertheless most food relationships are not simple food c h a ~ n sbut are more often complex as a result of opportunistic feedlng I3jCs could be a good ind~cator and/or a research tool for studies on food habits and Fig. 9 shows the annual variation of '37Cs in 24 fish specles after the Chernobyl accident (1987 to 1995). The effective environmental half-lives were calculated a n d the results a r e shown in Table 6. Species having positive Or negative annual trends ln their mean body weight or having a large yearly variation in mean body Tclcosts Species Fig 8. ~~~d habits a n d mean Ii'cs concentration factors for marine organisms. Vert~callines show standard dev~ation Kasamatsu & Ishikawa: '."CS concentrations in marine organisms - -- 00 ! 1984 I 1986 117 - 1988 1990 1992 1994 1996 Year Fig. 9. Yearly changes of mean concentrations of '"CS in 24 fish species. Lines are least squares fits to the data 1965, King 1964, Morgan 1964, Pendleton et al. 1965, Hasanen et al. 1968, Kolehmainen et al. 1968, Pentreath 1973, Kasamatsu 1996). Morgan (1964),Hiyama & Shimizu (1964), Morita (1980) and Yoshida (1992) suggested a positive correlation between body size and radiocesium concentration in fishes, while Hasanen & Miettinen (1963), Kimura (1984), Newman & Brisbin (1990), and Ishikawa et al. (1995) observed neither a positive nor any other clear correlation between '17Cs and size (or age) of fishes. However, the reason for this discrepancy has not been clearly identified. We also found both size-dependence and no size-dependence of '37Cs concentration in different fish species. Our analysis demonstrated that those different patterns were due to changes of food habits with growth. The I3?Cs concentration in the fish increased clearly when the food habit changed from low trophic level to high trophic level with growth, but it did not increase when the fish did not change their prey. These results suggest that food habit is one of the most important factors affecting concentrations of 137Csin marine fishes. The effect of food habits on '"CS concentration could explain the difference in 13'Cs concentration in different areas (see Table 4). It has been suggested that the difference of food of Atka mackerel from Hokkaido (mainly fishes) and Niigata (mainly zooplankton) might cause the difference in '"CS concentration between areas, because zooplankton has a much lower concentration of I3'Cs than fishes (Kasamatsu 1996).In the case of common Japanese conger, size-dependent concentration of '"'CS (Fig. 3) resulted in a high concentration in larger size fish (Fukui area) and a low concentration in smaller size fish (Miyagi area). The yearly variation of '"CS in stone flounders (Fig. 10) before 1992 was well explained by the yearly variation Table 6. Annual trends of '"'CS concentration in major fish species during 1987-1995 Species Sloped Halflife (yr) Stingrays Common Japanese conger ( M i y a g ~ ) Common Japanese conger (Fukui) Deep-sea smelt Pacific cod Walleye pollack (Hokkaido) Scorplon fish Black rockflsh Bertai.1 flathead Atka mackerel (Hokkaido) Japanese sea bass Jacks Red sea bream Crimson sea bream White croaker Rudder fish Japanese sandfish Bastard halibut Flathead flounder Shothole halibut Stone flounder Brown sole Black tonguefish Red tonguefish -0.045 -0.017 -0.049 -0.041 -0.092 -0.063 -0.053 -0.068 -0.052 -0.064 -0.075 -0.037 -0.079 -0.042 -0.052 -0.081 -0.055 -0.061 -0.063 -0.041 -0.078 -0.072 -0.057 -0.063 15 4 40 7 14 1 16.9 7.5 11.O 13.6 10 2 13 8 10.8 92 18.7 8.8 16.5 13.3 8.6 12.6 11.3 11 0 16.9 8.9 9.6 12.2 11.0 Corr. ~oeff.~ - No. of samples CV of body wtC Trend body wtd 17 9 18 11 35 16 21 15 15 11 46 15 27 18 11 0.49 0.42 0.19 0.29 0.51 0.4 1 0.36 0.21 0.47 0.18 0.40 0.31 0.49 0.30 0.21 0.36 0.26 0.85 0.32 0.19 0.73 0.27 0.23 0.25 No No No No No No No No No Posit~ve No Negative No No No No Positive No No No No No Positive No - 0.57' 0 35 0 39 0.6 0.55 0.87 ' 0.70 ' 0.95 0.47 0.79" 0.72" 0.57' 0.88" 0.56' 0.86" 0.82 0.62 0.63 0.67. 0.47' 0.52 0.70" 0.62 0.67" m m m m m 18 16 49 41 18 18 17 18 12 bCorrelation coefficient ( ' s i g n ~ f ~ c a natt 5% and "at 1 % level). 'Coefficient of variation of yearly a E x p o n e n t ~ acoefficient. l change of mean body weight. "Trend of yearly body weight Mar Ecol Prog Ser 160: 109-120, 1997 118 0.00 1984 - - c-- - Mcan body kngth 1986 1988 1990 1992 1994 0 1996 Year Fig. 10. Kareius bicoloratus. Yearly change of '37Cs concentration and mean body length of stone flounders of size together with the size-dependent concentration in this species (caused by change of food habits with growth, Figs. 3 & 5). Through our investigations of food habits it is possible to describe most of the concentration levels of '"CS in surface fishes (those that inhabit the surface layers a m Common conger - m 6 Bertail flathead 0 Japanese sea bass Atka mackerel I Stone , flounder , , 0 0 500 1 1000 Mean Body Weight (g) , 0 Brown , , , sole , 500 1 l000 Mean Body Weight (g) Fig 11 Relationship between weight of fish and S1'N (from Kasamatsu et al. unpubl.). Muscle samples for SI5N were frozen and 615N was measured using a Finnigan MAT Model delta E , following the method described in Minagabva & Wada (1984) with a sea temperature of approximately 10 to 25°C); however, we identified another group of fishes having relatively high concentration levels of '37Cs despite a low concentration in their food (e.g. walleye pollack, Atka mackerel, and deep-sea smelt, all of which inhabit deep-sea areas with a water temperature of less than 3 to 5OC), indicating that concentrations of '37Cs in these fishes could not be explained only through their food habits. Kolehmainen et al. (1968) and Cocchio et al. (1995) suggested a decrease of excretion rate (increased biological half-lives) when the difference of environmental temperature is more than 10°C. Because there is no information on the absorption rate of 137Csat low temperatures or in changing temperatures, it is not possible at this stage to make conclusions about factors affecting accumulation of 13'Cs in deep-sea fishes. However, it is reasonable to suggest that environmental conditions (e.g. sea temperature) together with biological conditions (e.g low food availability) may affect accumulation of '37Cs in these fishes. Since there is little information on the effect of depth of habitat (effect of temperature, difference of food or availability of food, etc.) on accumulation of radionuclides, especially for 13'Cs, this is a topic that should be investigated further. The natural variation of S'", which has recently been used to identify the trophic level of animals in relation to their food habits or trophic levels (Owens 1987, Wada et al. 1987, Fry 1988), was examined and its behavior compared in relation to food habits to that of '''CS. Fig. 11 shows the relationship between body weight and 615N in 10 fish species in which the '37Cs concentration was also measured. In common Japanese conger, Pacific cod, bartail flathead and stone flounder, which shift their food habits to a higher trophic level with growth, '37Cs concentration shows good agreement with the change of food habits according to growth (Figs. 2 & 3) but 61SN does not show a significant change with growth except Pacific cod. Because the biological half-life of 13'Cs is relatively short (approximately 100 d ; Gomez et al. 1991), concentration of 13'Cs in fishes may well reflect minor changes in prey species or variation of food quantity better than 615N. Acknowledgements. We express our thanks to R. Saito, 1. Ueda, Y. Nagaya, Y Suzuki. T Tomizawa, K. Yamada, N. Nonaka, T. Iba, K. Marurno, S. Maeda. S. Sakamoto, H. Kawamura, K. Kawabe, T. Harasaki and N. Inatomi of our Institute for their cooperation. We also express our thanks to P. Ensor and B. Casareto for their superb editing. We thank 3 anonymous reviewers for their useful comments. The study could not have been undertaken without the assistance and cooperation of the members of local fisherman's unions and the Japan Chemlcal Analysis Center This study was conducted as a part of a marine environmental radioactive monitoring program by the Science and Technology Agency of Japan. Kasamatsu & Ishikawa: Ii7Cs c:oncentrations in marine organisms LITERATURE CITED Baptist JP, Price TJ (1962) Accumulation and retention of 137Csby marine fishes. Fish Bull US 62:177-197 Bryan GW (1963) The accumulation of '"CS by brackish water invertebrates and its retention to the regulation of potassium and sodium. J Mar Biol Assoc UK 43:541-575 Bryan GW (1965) Ionic regulation in the squat lobster Golathea sqamlfera, with special reference to the relationship between potassium metabolism a n d the accumulation of radioactive caesium. 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